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Research Article

Validation of NAD synthase inhibitors for inhibiting the cell viability of Leishmania donovani: In silico and in vitro approach

, ORCID Icon, , &
Pages 4481-4493 | Received 17 Jul 2018, Accepted 16 Nov 2018, Published online: 19 Jan 2019

References

  • Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindahl, E. (2015). GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1–2, 19–25.
  • Akpunarlieva, S., Weidt, S., Lamasudin, D., Naula, C., Henderson, D., Barrett, M., … Burchmore, R. (2017). Integration of proteomics and metabolomics to elucidate metabolic adaptation in Leishmania. Journal of Proteomics, 155, 85–98. doi:10.1016/j.jprot.2016.12.009
  • Aronson, N., Herwaldt, B. L., Libman, M., Pearson, R., Lopez-Velez, R., Weina, P., … Magill, A. (2016). Diagnosis and treatment of leishmaniasis: Clinical practice guidelines by the Infectious Diseases Society of America (IDSA) and the American Society of Tropical Medicine and Hygiene (ASTMH). Clinical Infectious Diseases, 63(12), 1539–1557. doi:10.1093/cid/ciw742
  • Belenky, P., Racette, F. G., Bogan, K. L., McClure, J. M., Smith, J. S., & Brenner, C. (2007). Nicotinamide riboside promotes Sir2 silencing and extends lifespan via Nrk and Urh1/Pnp1/Meu1 pathways to NAD+. Cell, 129(3), 473–484. doi:10.1016/j.cell.2007.03.024
  • Bieganowski, P., & Brenner, C. (2004). Discoveries of nicotinamide riboside as a nutrient and conserved NRK genes establish a Preiss–Handler independent route to NAD + in fungi and humans. Cell, 117(4), 495–502.
  • Boshoff, H. I. M., Xu, X., Tahlan, K., Dowd, C. S., Pethe, K., Camacho, L. R., … Barry, C. E. (2008). Biosynthesis and recycling of nicotinamide cofactors in Mycobacterium tuberculosis an essential role for NAD in nonreplicating bacilli. Journal of Biological Chemistry, 283(28), 19329–19341.
  • Chakrabarti, G., Basu, A., Manna, P. P., Mahato, S. B., Mandal, N. B., & Bandyopadhyay, S. (1999). Indolylquinoline derivatives are cytotoxic to Leishmania donovani promastigotes and amastigotes in vitro and are effective in treating murine visceral leishmaniasis. Journal of Antimicrobial Chemotherapy, 43(3), 359–366. doi:10.1093/jac/43.3.359
  • Chawla, B., & Madhubala, R. (2010). Drug targets in leishmania. Journal of Parasitic Diseases : Official Organ of the Indian Society for Parasitology, 34(1), 1–13.
  • Colovos, C., & Yeates, T. O. (1993). Verification of protein structures: Patterns of nonbonded atomic interactions. Protein Science, 2(9), 1511–1519. doi:10.1002/pro.5560020916
  • Corral, M. J., Gonzalez-Sanchez, E., Cuquerella, M., & Alunda, J. M. (2014). In vitro synergistic effect of amphotericin B and allicin on Leishmania donovani and L. infantum. Antimicrobial Agents and Chemotherapy, 58(3), 1596–1602. doi:10.1128/AAC.00710-13
  • Croft, S. L., Sundar, S., & Fairlamb, A. H. (2006). Drug resistance in leishmaniasis. Clinical Microbiology Reviews, 19(1), 111–126. doi:10.1128/CMR.19.1.111-126.2006
  • Eisenberg, D., Lüthy, R., & Bowie, J. U. (1997). VERIFY3D: Assessment of protein models with three-dimensional profiles. Methods in Enzymology (Vol. 277, pp. 396–404). Amsterdam, Netherlands: Elsevier.
  • El Fadili, K., Messier, N., Leprohon, P., Roy, G., Guimond, C., Trudel, N., … Ouellette, M. (2005). Role of the ABC transporter MRPA (PGPA) in antimony resistance in Leishmania infantum axenic and intracellular amastigotes. Antimicrobial Agents and Chemotherapy, 49(5), 1988–1993.
  • Escobar, P., Matu, S., Marques, C., & Croft, S. L. (2002). Sensitivities of Leishmania species to hexadecylphosphocholine (miltefosine), ET-18-OCH(3) (edelfosine) and amphotericin B. Acta Tropica, 81(2), 151–157.
  • Espey, M. G., & Namboodiri, M. A. (2000). Selective metabolism of kynurenine in the spleen in the absence of indoleamine 2,3-dioxygenase induction. Immunology Letters, 71(1), 67–72.
  • Gazanion, E., Garcia, D., Silvestre, R., Gérard, C., Guichou, J. F., Labesse, G., … Vergnes, B. (2011). The Leishmania nicotinamidase is essential for NAD + production and parasite proliferation. Molecular Microbiology, 82(1), 21–38.
  • Gazzaniga, F., Stebbins, R., Chang, S. Z., McPeek, M. A., & Brenner, C. (2009). Microbial NAD metabolism: Lessons from comparative genomics. Microbiology and Molecular Biology Reviews, 73(3), 529–541.
  • Ghorbani, M., & Farhoudi, R. (2018). Leishmaniasis in humans: Drug or vaccine therapy? Drug Design, Development and Therapy, 12, 25–40. doi:10.2147/dddt.S146521
  • Irigoin, F., Cibils, L., Comini, M. A., Wilkinson, S. R., Flohe, L., & Radi, R. (2008). Insights into the redox biology of Trypanosoma cruzi: Trypanothione metabolism and oxidant detoxification. Free Radical Biology & Medicine, 45(6), 733–742. doi:10.1016/j.freeradbiomed.2008.05.028
  • Jain, V., & Jain, K. (2018). Molecular targets and pathways for the treatment of visceral leishmaniasis. Drug Discovery Today, 23(1), 161–170. doi:10.1016/j.drudis.2017.09.006
  • Kamhawi, S. (2006). Phlebotomine sand flies and Leishmania parasites: Friends or foes? Trends in Parasitology, 22(9), 439–445. doi:10.1016/j.pt.2006.06.012
  • Krauth-Siegel, R. L., & Comini, M. A. (2008). Redox control in trypanosomatids, parasitic protozoa with trypanothione-based thiol metabolism. Biochimica et Biophysica Acta, 1780(11), 1236–1248.
  • Kumari, R., Kumar, R., Consortium, O. S. D. D., & Lynn, A. (2014). g_mmpbsa-a GROMACS tool for high-throughput MM-PBSA calculations . Journal of Chemical Information and Modeling, 54(7), 1951–1962.
  • Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26(2), 283–291. doi:10.1107/S0021889892009944
  • Leroux, A. E., Maugeri, D. A., Cazzulo, J. J., & Nowicki, C. (2011). Functional characterization of NADP-dependent isocitrate dehydrogenase isozymes from Trypanosoma cruzi. Molecular and Biochemical Parasitology, 177(1), 61–64.
  • Ma, B., Pan, S. J., Zupancic, M. L., & Cormack, B. P. (2007). Assimilation of NAD(+) precursors in Candida glabrata. Molecular Microbiology, 66(1), 14–25. doi:10.1111/j.1365-2958.2007.05886.x
  • Maarouf, M., Adeline, M., Solignac, M., Vautrin, D., & Robert-Gero, M. (1998). Development and characterization of paromomycin-resistant Leishmania donovani promastigotes. Parasite, 5(2), 167–173.
  • Maltezou, H. C. (2009). Drug resistance in visceral leishmaniasis. BioMed Research International, 2010, 8.
  • Mbongo, N., Loiseau, P. M., Billion, M. A., & Robert-Gero, M. (1998). Mechanism of amphotericin B resistance in Leishmania donovani promastigotes. Antimicrobial Agents and Chemotherapy, 42(2), 352–357.
  • Meier, A., Erler, H., & Beitz, E. (2018). Targeting channels and transporters in protozoan parasite infections. Frontiers in Chemistry, 6, 88. doi:10.3389/fchem.2018.00088
  • Michels, P. A., & Avilán, L. (2011). The NAD + metabolism of leishmania, notably the enzyme nicotinamidase involved in NAD + salvage, offers prospects for development of anti‐parasite chemotherapy. Molecular Microbiology, 82(1), 4–8.
  • Mohapatra, S. (2014). Drug resistance in leishmaniasis: Newer developments. Tropical Parasitology, 4(1), 4–9. doi:10.4103/2229-5070.129142
  • Mori, V., Amici, A., Mazzola, F., Di Stefano, M., Conforti, L., Magni, G., … Orsomando, G. (2014). Metabolic profiling of alternative NAD biosynthetic routes in mouse tissues. PLoS One, 9(11), e113939.
  • Moro, W. B., Yang, Z., Kane, T. A., Brouillette, C. G., & Brouillette, W. J. (2009). Virtual screening to identify lead inhibitors for bacterial NAD synthetase (NADs). Bioorganic & Medicinal Chemistry Letters, 19(7), 2001–2005.
  • Moro, W. B., Yang, Z., Kane, T. A., Zhou, Q., Harville, S., Brouillette, C. G., & Brouillette, W. J. (2009). SAR studies for a new class of antibacterial NAD biosynthesis inhibitors. Journal of Combinatorial Chemistry, 11(4), 617–625. doi:10.1021/cc9000357
  • Mwenechanya, R., Kovářová, J., Dickens, N. J., Mudaliar, M., Herzyk, P., Vincent, I. M., … Barrett, M. P. (2017). Sterol 14α-demethylase mutation leads to amphotericin B resistance in Leishmania mexicana. PLoS Neglected Tropical Diseases, 11(6), e0005649.
  • Nikiforov, A., Dolle, C., Niere, M., & Ziegler, M. (2011). Pathways and subcellular compartmentation of NAD biosynthesis in human cells: From entry of extracellular precursors to mitochondrial NAD generation. Journal of Biological Chemistry, 286(24), 21767–21778. doi:10.1074/jbc.M110.213298
  • Nikiforov, A., Kulikova, V., & Ziegler, M. (2015). The human NAD metabolome: Functions, metabolism and compartmentalization. Critical Reviews in Biochemistry and Molecular Biology, 50(4), 284–297. doi:10.3109/10409238.2015.1028612
  • O'Hara, J. K., Kerwin, L. J., Cobbold, S. A., Tai, J., Bedell, T. A., Reider, P. J., & Llinás, M. (2014). Targeting NAD + metabolism in the human malaria parasite Plasmodium falciparum. PLoS One, 9(4), e94061.
  • Panozzo, C., Nawara, M., Suski, C., Kucharczyka, R., Skoneczny, M., Bécam, A. M., … Herbert, C. J. (2002). Aerobic and anaerobic NAD + metabolism in Saccharomyces cerevisiae. FEBS Letters, 517(1–3), 97–102.
  • Pérez-Victoria, F. J., Gamarro, F., Ouellette, M., & Castanys, S. (2003). Functional cloning of the miltefosine transporter A novel P-type phospholipid translocase from leishmania involved in drug resistance. Journal of Biological Chemistry, 278(50), 49965–49971.
  • Preiss, J., & Handler, P. (1958). Biosynthesis of diphosphopyridine nucleotide II. Enzymatic aspects. Journal of Biological Chemistry, 233(2), 493–500.
  • Purkait, B., Kumar, A., Nandi, N., Sardar, A. H., Das, S., Kumar, S., … Das, P. (2012). Mechanism of amphotericin B resistance in clinical isolates of Leishmania donovani. Antimicrobial Agents and Chemotherapy, 56(2), 1031–1041.
  • Rodionova, I. A., Schuster, B. M., Guinn, K. M., Sorci, L., Scott, D. A., Li, X., …., Locher, C. (2014). Metabolic and bactericidal effects of targeted suppression of NadD and NadE enzymes in mycobacteria. MBio, 5(1), e00747–e00713.
  • Rongvaux, A., Andris, F., Van Gool, F., & Leo, O. (2003). Reconstructing eukaryotic NAD metabolism. BioEssays, 25(7), 683–690. doi:10.1002/bies.10297
  • Saravanan, V., & Das, P. (2018). Recent progress in drug targets and inhibitors towards combating leishmaniasis. Acta Tropica, 181, 95–104.
  • Shaked-Mishan, P., Ulrich, N., Ephros, M., & Zilberstein, D. (2001). Novel intracellular SbV reducing activity correlates with antimony susceptibility in Leishmania donovani. Journal of Biological Chemistry, 276(6), 3971–3976.
  • Singh, A., Kaushik, R., Mishra, A., Shanker, A., & Jayaram, B. (2016). ProTSAV: A protein tertiary structure analysis and validation server. Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics, 1864(1), 11–19.
  • Singh, N., Kumar, M., & Singh, R. K. (2012). Leishmaniasis: Current status of available drugs and new potential drug targets. Asian Pacific Journal of Tropical Medicine, 5(6), 485–497. doi:10.1016/S1995-7645(12)60084-4
  • Soares, M. B. P., Silva, C. V., Bastos, T. M., Guimarães, E. T., Figueira, C. P., Smirlis, D., & Azevedo, W. F. (2012). Anti-Trypanosoma cruzi activity of nicotinamide. Acta Tropica, 122(2), 224–229.
  • Sorci, L., Martynowski, D., Rodionov, D. A., Eyobo, Y., Zogaj, X., Klose, K. E., … Osterman, A. L. (2009). Nicotinamide mononucleotide synthetase is the key enzyme for an alternative route of NAD biosynthesis in Francisella tularensis. Proceedings of the National Academy of Sciences, 106(9), 3083–3088.
  • Sundar, S., & Singh, B. (2018). Emerging therapeutic targets for treatment of leishmaniasis. Expert Opinion on Therapeutic Targets, 22(6), 467–486. doi:10.1080/14728222.2018.1472241
  • van Aalten, D. M., Bywater, R., Findlay, J. B., Hendlich, M., Hooft, R. W., & Vriend, G. (1996). PRODRG, a program for generating molecular topologies and unique molecular descriptors from coordinates of small molecules. Journal of Computer-Aided Molecular Design, 10(3), 255–262. doi:10.1007/BF00355047
  • van Griensven, J., Balasegaram, M., Meheus, F., Alvar, J., Lynen, L., & Boelaert, M. (2010). Combination therapy for visceral leishmaniasis. Lancet Infectious Diseases, 10(3), 184–194.
  • Velu, S. E., Mou, L., Luan, C. H., Yang, Z. W., DeLucas, L. J., Brouillette, C. G., & Brouillette, W. J. (2007). Antibacterial nicotinamide adenine dinucleotide synthetase inhibitors: Amide- and ether-linked tethered dimers with alpha-amino acid end groups. Journal of Medicinal Chemistry, 50(11), 2612–2621. doi:10.1021/jm061349l
  • Wang, X., Ahn, Y.-M., Lentscher, A. G., Lister, J. S., Brothers, R. C., Kneen, M. M., … Dowd, C. S. (2017). Design, synthesis, and evaluation of substituted nicotinamide adenine dinucleotide (NAD+) synthetase inhibitors as potential antitubercular agents. Bioorganic & Medicinal Chemistry Letters, 27(18), 4426–4430.
  • Webb, B., & Sali, A. (2016). Comparative protein structure modeling using MODELLER. Current Protocols in Protein Science, 54, 5.6.1–5.6.37.
  • Werbovetz, K. A. (2000). Target-based drug discovery for malaria, leishmaniasis, and trypanosomiasis. Current Medicinal Chemistry, 7(8), 835–860.
  • Xu, D., & Zhang, Y. (2011). Improving the physical realism and structural accuracy of protein models by a two-step atomic-level energy minimization. Biophysical Journal., 101(10), 2525–2534.
  • Yang, J., & Zhang, Y. (2015). Protein structure and function prediction using I-TASSER. Current Protocols in Bioinformatics, 52, 5.8.1–5.8.15. doi:10.1002/0471250953.bi0508s52

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